Cooperation and Bacterial Pathogenicity: an Approach to Social Evolution C Alfonso Molina1,3* and Susana Vilchez2
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Molina and Vilchez Revista Chilena de Historia Natural 2014, 87:14 http://www.revchilhistnat.com/content/87/1/14 REVIEW Open Access Cooperation and bacterial pathogenicity: an approach to social evolution C Alfonso Molina1,3* and Susana Vilchez2 Abstract Kin selection could provide an explanation for social behavior in bacteria. The production of public goods such as extracellular molecules is metabolically costly for bacteria but could help them to exploit nutrients or invade a host. Some bacterial cells called social cheaters do not produce public goods; however, they take advantage of these extracellular molecules. In this review, the relationships between social behavior, cooperation, and evolution of bacterial pathogenicity are analyzed. This paper also examines the role of horizontal transfer of genes encoding for virulence factors and how the movement of mobile genetic elements would influence the pathogenicity and social relationships. Moreover, the link between ecological relationships and evolution in entomopathogenic bacteria, focusing on Bacillus thuringiensis is considered. Finally, the findings obtained with B. thuringiensis are extrapolated on Bacillus pumilus 15.1, an entomopathogenic strain whose pathogenicity is not understood yet. Keywords: Cooperation; Evolution; Pathogenicity; Public goods; Sociability Introduction (Brown 1999), adhesive polymers (Rainey and Rainey The social relationships of microorganisms are based on 2003), or siderophores (West and Buckling 2003), amongst a wide range of extracellular actions produced by indi- others. This social behavior is, from a metabolic point of vidual cells, which can affect the reproductive efficiency view, costly for the individual cells, although it is beneficial of other nearby cells. The production of molecules such for the group. However, certain cells, known as ‘cheaters’ as enzymes or chelants, which allow for the exploitation can decide not to produce these beneficial molecules for of nutrients that would not otherwise be accessible, or the group and instead take advantage of the rewards of the formation of multicellular structures, are examples social actions without paying any cost (West et al. 2006). of this kind of action (Buckling and Rainey 2002; Griffin Thus, in microorganisms, social cheaters that do not dis- et al. 2004; West et al. 2006). Extracellular products and play cooperative behavior are considered mutants (West other resources are public goods that may be used by et al. 2007; Wakano et al. 2009; Foster 2010; Smith et al. the individual that produces them or by all individuals of 2014) and can evolve with relative speed if they are favor- the group or population (West et al. 2006, 2007). For ably selected (Velicer et al. 2000; Rainey and Rainey 2003; example, bacteria produce numerous factors that are Foster et al. 2004; Griffin et al. 2004; Dugatkin et al. 2005; considered to be public goods and are released into the Harrison and Buckling 2005). environment, such as quorum-sensing molecules (Daniels Evolution experiments conducted on a wide range of et al. 2003; Diggle et al. 2007a; Williams et al. 2007), mem- microorganisms have demonstrated that this kind of brane vesicles (Schooling and Beveridge 2006), microbial cooperative behavior is most prevalent when there is a repellents (Burgess et al. 2003), host manipulation factors high degree of genetic closeness between the cells (West et al. 2006; Mitri et al. 2011). For example, the opportunis- tic pathogen Pseudomonas aeruginosa (Schroeter, 1872) * Correspondence: [email protected] 1Facultad de Ciencias Ambientales, Universidad Internacional SEK, Calle produces extracellular iron-chelating molecules, known as Alberto Einstein y 5ta. Transversal, Campus Miguel de Cervantes, Carcelén, siderophores (West and Buckling 2003). These molecules Quito 170120, Ecuador are iron-scavenging agents that are released into the envir- 3Centro Internacional de Zoonosis, Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador (UC), PO Box.17-03-100, Quito, onment in response to a lack of this element (Ratledge Ecuador and Dover 2000). The siderophores high affinity for iron Full list of author information is available at the end of the article © 2014 Molina and Vilchez; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Molina and Vilchez Revista Chilena de Historia Natural 2014, 87:14 Page 2 of 9 http://www.revchilhistnat.com/content/87/1/14 enables them to capture the metal from compounds such cooperate to form eukaryotic cells, cells cooperate to as ferrous hydroxide and host organism proteins such as form multicellular organisms, pathogenic bacteria cooper- transferrin or ferritin (Neilands 1995; Drechsel and Jung ate to overcome the defenses of their hosts, animals feed 1998). In addition, the relationship between siderophore cooperatively, and humans and some species of insect co- production and bacterial growth rate suggests that the operate to construct societies (West et al. 2006, 2007). production of siderophores contributes to bacterial viru- With regard to the cooperation of pathogenic bacteria, lence (West and Buckling 2003). Some cells have evolved reproduction within the host can be a cooperative activity as social cheaters since they produce small quantities of that involves the secretion of virulent factors whose bene- siderophores and yet they benefit from the action of side- fits can be shared by all of the cells, whether they secrete rophores produced by other cells (Ross-Gillespie et al. them or not (Smith 2001). In this way, cooperation and 2007; Mitri et al. 2011). Using this strategy, the cheats success in overcoming the host's defenses will depend on increase their frequency in comparison with the wild the nature of the virulence factor (public good) as well as genotype (that does produce the molecule) (Mitri et al. the proportion of social cheaters present in a population. 2011; Smith et al. 2014). However, in order for sidero- For example, this could explain why the enterotoxigenic phore production to remain high, populations must be Escherichia coli (Migula, 1895) (producer of LT and ST exposed to a strong genetic bottleneck, which ensures that toxins) requires a greater population density to cause an the genetic relationship between the cells that produces infection when compared with the enterohemorrhagic E. the chelating agent and the one that is not is high. There coli, a producer of Shiga toxin (STX) (Smith and Halls are numerous examples of the role of kin selection in 1968; O'brien et al. 1984), which requires a smaller num- explaining the cooperation between microorganisms, such ber of cells. Enterohemorrhagic E. coli populations would as the example of Bacillus subtilis (Ehrenberg, 1835), therefore include a lower proportion of cheater cells. which forms biofilms in which closely related cells cooper- Although there is no doubt about cooperative behavior, ate by becoming differentiated and sharing out functions there is controversy on how this kind of behavior might (Foster 2010). This same kind of social behavior has been be interpreted, via kin selection or via group selection reported in various other species (Wakano et al. 2009). (West et al. 2007; Wilson 2008). As mentioned above, This sacrificial phenomenon does not occur in multi- there are various pieces of evidence that support the idea cellular organisms since the cells do not differ genetic- that this kind of behavior in bacteria could be explained ally from one another. No cell has an advantage over by the kin selection theory. For example, in bacterial spe- another, and if any cell should vary, it would be excluded cies that form biofilms, cells that are genetically related from the cell line. For this reason, the deception of indi- are found close to one another (Griffin et al. 2004; Diggle vidual cells is restricted in the majority of multicellular et al. 2007a,b). Nevertheless, the fact that all of the cells organisms (Kessin 2000). However, there is another originate from a single mother cell in the majority of bio- route to multicellularity that is adopted by organisms films has been presented as an argument in favor of group such as Dictyostelium or Myxococus (a group of social selection (West et al. 2006; Boyle et al. 2013; Drescher bacteria). When nutrients become limited and cell dens- et al. 2013). ity is high, Myxococcus xanthus (Beebe, 1941) activates Biofilms are communities of microbial cells, commonly various genes that break up the aggregation of local composed of various lineages or species, which grow on groups that exchange intercellular signals, allowing the surfaces surrounded by polymers (Kolenbrander 2000; formation of spore-producing fruiting bodies (Kadam and Hall-Stoodley et al. 2004). In this kind of community, the Velicer 2006). These fruiting bodies contain approximately cellular groups have limited space and influence each 50,000 cells, but only a fraction of the cells have differenti- other depending on the distance between them. These ated latent myxospores (Curtis et al. 2007) which appar- spatial relationships are of the utmost importance for the ently sacrifice themselves for the common good (Fiegna compression of cellular community cooperation evolution and Velicer 2006; Fiegna et al. 2006; Kadam